-
COVID-19 vaccine effectiveness against symptomatic infection with SARS-CoV-2 BA.1/BA.2 lineages among adults and adolescents in a multicentre primary care study, Europe, December 2021 to June 2022
- Charlotte Lanièce Delaunay1 , Iván Martínez-Baz2,3 , Noémie Sève4 , Lisa Domegan5 , Clara Mazagatos6 , Silke Buda7 , Adam Meijer8 , Irina Kislaya9 , Catalina Pascu10 , AnnaSara Carnahan11 , Beatrix Oroszi12 , Maja Ilić13 , Marine Maurel1 , Aryse Melo9 , Virginia Sandonis Martín14 , Camino Trobajo-Sanmartín2,3 , Vincent Enouf15,16 , Adele McKenna5 , Gloria Pérez-Gimeno6 , Luise Goerlitz7 , Marit de Lange8 , Ana Paula Rodrigues9 , Mihaela Lazar10 , Neus Latorre-Margalef11 , Gergő Túri12 , Jesús Castilla2,3 , Alessandra Falchi17 , Charlene Bennett18 , Virtudes Gallardo19 , Ralf Dürrwald20 , Dirk Eggink8 , Raquel Guiomar9 , Rodica Popescu21 , Maximilian Riess11 , Judit Krisztina Horváth12 , Itziar Casado2,3 , Mª del Carmen García22 , Mariëtte Hooiveld23 , Ausenda Machado9 , Sabrina Bacci24 , Marlena Kaczmarek24 , Esther Kissling1 , on behalf of the European Primary Care Vaccine Effectiveness Group25
-
View Affiliations Hide AffiliationsAffiliations: 1 Epiconcept, Paris, France 2 Instituto de Salud Pública de Navarra – IdiSNA, Pamplona, Spain 3 Consortium for Biomedical Research in Epidemiology and Public Health (CIBERESP), Madrid, Spain 4 Sorbonne Université, INSERM, Institut Pierre Louis d'épidémiologie et de Santé Publique (IPLESP UMRS 1136), Paris, France 5 Health Protection Surveillance Centre, Dublin, Ireland 6 National Centre of Epidemiology, CIBERESP, Carlos III Health Institute, Madrid, Spain 7 Department for Infectious Disease Epidemiology, Respiratory Infections Unit, Robert Koch Institute, Berlin, Germany 8 National Institute for Public Health and the Environment (RIVM), Bilthoven, the Netherlands 9 Instituto Nacional de Saúde Dr. Ricardo Jorge, Lisbon, Portugal 10 Cantacuzino National Military Medical Institute for Research and Development, Bucharest, Romania 11 Public Health Agency of Sweden, Stockholm, Sweden 12 National Laboratory for Health Security, Epidemiology and Surveillance Centre, Semmelweis University, Budapest, Hungary 13 Croatian Institute of Public Health (CIPH), Zagreb, Croatia 14 National Centre for Microbiology, Carlos III Health Institute, Madrid, Spain 15 Institut Pasteur, Pasteur International Bioresources network (PIBnet), Plateforme de Microbiologie Mutualisée (P2M), Paris, France 16 Institut Pasteur, Centre National de Référence Virus des Infections Respiratoires (CNR VIR), Paris, France 17 Laboratoire de Virologie, Université de Corse-Inserm, Corte, France 18 National Virus Reference Laboratory, University College Dublin, Dublin, Ireland 19 Dirección General de Salud Pública y Ordenación Farmacéutica, Junta de Andalucía, Sevilla, Spain 20 National Reference Centre for Influenza, Robert Koch Institute, Berlin, Germany 21 National Institute of Public Health, Bucharest, Romania 22 Subdirección de Epidemiología, Dirección General de Salud Pública, Servicio Extremeño de Salud, Mérida, Spain 23 Nivel, Utrecht, the Netherlands 24 European Centre for Disease Prevention and Control, Stockholm, Sweden 25 The members of the group are listed under AcknowledgementsEsther Kisslinge.kissling epiconcept.fr
-
View Citation Hide Citation
Citation style for this article: Lanièce Delaunay Charlotte, Martínez-Baz Iván, Sève Noémie, Domegan Lisa, Mazagatos Clara, Buda Silke, Meijer Adam, Kislaya Irina, Pascu Catalina, Carnahan AnnaSara, Oroszi Beatrix, Ilić Maja, Maurel Marine, Melo Aryse, Sandonis Martín Virginia, Trobajo-Sanmartín Camino, Enouf Vincent, McKenna Adele, Pérez-Gimeno Gloria, Goerlitz Luise, de Lange Marit, Rodrigues Ana Paula, Lazar Mihaela, Latorre-Margalef Neus, Túri Gergő, Castilla Jesús, Falchi Alessandra, Bennett Charlene, Gallardo Virtudes, Dürrwald Ralf, Eggink Dirk, Guiomar Raquel, Popescu Rodica, Riess Maximilian, Horváth Judit Krisztina, Casado Itziar, García Mª del Carmen , Hooiveld Mariëtte, Machado Ausenda, Bacci Sabrina, Kaczmarek Marlena, Kissling Esther, on behalf of the European Primary Care Vaccine Effectiveness Group. COVID-19 vaccine effectiveness against symptomatic infection with SARS-CoV-2 BA.1/BA.2 lineages among adults and adolescents in a multicentre primary care study, Europe, December 2021 to June 2022. Euro Surveill. 2024;29(13):pii=2300403. https://doi.org/10.2807/1560-7917.ES.2024.29.13.2300403 Received: 28 Jul 2023; Accepted: 14 Dec 2023
- Previous Article
- Table of Contents
- Next Article
Abstract
Scarce European data in early 2021 suggested lower vaccine effectiveness (VE) against SARS-CoV-2 Omicron lineages than previous variants.
We aimed to estimate primary series (PS) and first booster VE against symptomatic BA.1/BA.2 infection and investigate potential biases.
This European test-negative multicentre study tested primary care patients with acute respiratory symptoms for SARS-CoV-2 in the BA.1/BA.2-dominant period. We estimated PS and booster VE among adults and adolescents (PS only) for all products combined and for Comirnaty alone, by time since vaccination, age and chronic condition. We investigated potential bias due to correlation between COVID-19 and influenza vaccination and explored effect modification and confounding by prior SARS-CoV-2 infection.
Among adults, PS VE was 37% (95% CI: 24–47%) overall and 60% (95% CI: 44–72%), 43% (95% CI: 26–55%) and 29% (95% CI: 13–43%) < 90, 90–179 and ≥ 180 days post vaccination, respectively. Booster VE was 42% (95% CI: 32–51%) overall and 56% (95% CI: 47–64%), 22% (95% CI: 2–38%) and 3% (95% CI: −78% to 48%), respectively. Primary series VE was similar among adolescents. Restricting analyses to Comirnaty had little impact. Vaccine effectiveness was higher among older adults. There was no signal of bias due to correlation between COVID-19 and influenza vaccination. Confounding by previous infection was low, but sample size precluded definite assessment of effect modification.
Primary series and booster VE against symptomatic infection with BA.1/BA.2 ranged from 37% to 42%, with similar waning post vaccination. Comprehensive data on previous SARS-CoV-2 infection would help disentangle vaccine- and infection-induced immunity.
Article metrics loading...
Full text loading...
References
-
European Medicines Agency (EMA). Authorised COVID-19 vaccines. Amsterdam: EMA. [Accessed: 21 Mar 2024]. Available from: https://www.ema.europa.eu/en/human-regulatory/overview/public-health-threats/coronavirus-disease-covid-19/treatments-vaccines/vaccines-covid-19/covid-19-vaccines-authorised
-
Kissling E, Hooiveld M, Martínez-Baz I, Mazagatos C, William N, Vilcu AM, et al. Effectiveness of complete primary vaccination against COVID-19 at primary care and community level during predominant Delta circulation in Europe: multicentre analysis, I-MOVE-COVID-19 and ECDC networks, July to August 2021. Euro Surveill. 2022;27(21):2101104. https://doi.org/10.2807/1560-7917.ES.2022.27.21.2101104 PMID: 35620997
-
Halloran ME, Longini IM, Struchiner CJ. Design and analysis of vaccine studies. New York: Springer; 2010. 387 p. https://doi.org/10.1007/978-0-387-68636-3
-
Sullivan SG, Tchetgen Tchetgen EJ, Cowling BJ. Theoretical basis of the test-negative study design for assessment of influenza vaccine effectiveness. Am J Epidemiol. 2016;184(5):345-53. https://doi.org/10.1093/aje/kww064 PMID: 27587721
-
Doll MK, Pettigrew SM, Ma J, Verma A. Effects of confounding bias in coronavirus disease 2019 (COVID-19) and influenza vaccine effectiveness test-negative designs due to correlated influenza and COVID-19 vaccination behaviors. Clin Infect Dis. 2022;75(1):e564-71. https://doi.org/10.1093/cid/ciac234 PMID: 35325923
-
Grochowska M, Ratajczak A, Zdunek G, Adamiec A, Waszkiewicz P, Feleszko W. A comparison of the level of acceptance and hesitancy towards the influenza vaccine and the forthcoming COVID-19 vaccine in the medical community. Vaccines (Basel). 2021;9(5):475. https://doi.org/10.3390/vaccines9050475 PMID: 34066790
-
Li M, Luo Y, Watson R, Zheng Y, Ren J, Tang J, et al. Healthcare workers’ (HCWs) attitudes and related factors towards COVID-19 vaccination: a rapid systematic review. Postgrad Med J. 2023;99(1172):520-8. https://doi.org/10.1136/postgradmedj-2021-140195 PMID: 37319159
-
Wang Q, Yang L, Jin H, Lin L. Vaccination against COVID-19: A systematic review and meta-analysis of acceptability and its predictors. Prev Med. 2021;150:106694. https://doi.org/10.1016/j.ypmed.2021.106694 PMID: 34171345
-
Ioannidis JPA. Factors influencing estimated effectiveness of COVID-19 vaccines in non-randomised studies. BMJ Evid Based Med. 2022;27(6):324-9. https://doi.org/10.1136/bmjebm-2021-111901 PMID: 35338091
-
Lewnard JA, Tedijanto C, Cowling BJ, Lipsitch M. Measurement of vaccine direct effects under the test-negative design. Am J Epidemiol. 2018;187(12):2686-97. https://doi.org/10.1093/aje/kwy163 PMID: 30099505
-
Powell AA, Kirsebom F, Stowe J, Ramsay ME, Lopez-Bernal J, Andrews N, et al. Protection against symptomatic infection with delta (B.1.617.2) and omicron (B.1.1.529) BA.1 and BA.2 SARS-CoV-2 variants after previous infection and vaccination in adolescents in England, August, 2021–March, 2022: a national, observational, test-negative, case-control study. Lancet Infect Dis. 2023;23(4):435-44. PMID: 36436536
-
Buchan SA, Chung H, Brown KA, Austin PC, Fell DB, Gubbay JB, et al. Estimated effectiveness of COVID-19 vaccines against omicron or delta symptomatic infection and severe outcomes. JAMA Netw Open. 2022;5(9):e2232760. https://doi.org/10.1001/jamanetworkopen.2022.32760 PMID: 36136332
-
Chung H, He S, Nasreen S, Sundaram ME, Buchan SA, Wilson SE, et al. Effectiveness of BNT162b2 and mRNA-1273 covid-19 vaccines against symptomatic SARS-CoV-2 infection and severe covid-19 outcomes in Ontario, Canada: test negative design study. BMJ. 2021;374:n1943. https://doi.org/10.1136/bmj.n1943 PMID: 34417165
-
Fiolet T, Kherabi Y, MacDonald CJ, Ghosn J, Peiffer-Smadja N. Comparing COVID-19 vaccines for their characteristics, efficacy and effectiveness against SARS-CoV-2 and variants of concern: a narrative review. Clin Microbiol Infect. 2022;28(2):202-21. https://doi.org/10.1016/j.cmi.2021.10.005 PMID: 34715347
-
Mohammed H, Pham-Tran DD, Yeoh ZYM, Wang B, McMillan M, Andraweera PH, et al. A systematic review and meta-analysis on the real-world effectiveness of COVID-19 vaccines against infection, symptomatic and severe COVID-19 disease caused by the Omicron variant (B.1.1.529). Vaccines (Basel). 2023;11(2):224. https://doi.org/10.3390/vaccines11020224 PMID: 36851102
-
Kissling E, Pozo F, Martínez-Baz I, Buda S, Vilcu AM, Domegan L, et al. Influenza vaccine effectiveness against influenza A subtypes in Europe: Results from the 2021-2022 I-MOVE primary care multicentre study. Influenza Other Respir Viruses. 2023;17(1):e13069. https://doi.org/10.1111/irv.13069 PMID: 36702797
-
Kissling E, Hooiveld M, Sandonis Martín V, Martínez-Baz I, William N, Vilcu AM, et al. Vaccine effectiveness against symptomatic SARS-CoV-2 infection in adults aged 65 years and older in primary care: I-MOVE-COVID-19 project, Europe, December 2020 to May 2021. Euro Surveill. 2021;26(29):2100670. https://doi.org/10.2807/1560-7917.ES.2021.26.29.2100670 PMID: 34296676
-
Valenciano M, Ciancio BC. on behalf of the I-MOVE study team C. I-MOVE: a European network to measure the effectiveness of influenza vaccines. Euro Surveill. 2012;17(39):20281. https://doi.org/10.2807/ese.17.39.20281-en PMID: 23041022
-
European Commission. Commission Implementing Decision (EU) 2018/945 of 22 June 2018 on the communicable diseases and related special health issues to be covered by epidemiological surveillance as well as relevant case definitions (Text with EEA relevance.). Official Journal of the European Union. Luxembourg: Publications Office of the European Union 6.7.2018:L 170/1. Available from: https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX%3A32018D0945&from=EN%29
-
European Centre for Disease Prevention and Control (ECDC). Data on SARS-CoV-2 variants in the EU/EEA. Stockholm: ECDC; 2023. Available from: https://www.ecdc.europa.eu/en/publications-data/data-virus-variants-covid-19-eueea
-
Firth D. Bias reduction of maximum likelihood estimates. Biometrika. 1993;80(1):27-38. https://doi.org/10.1093/biomet/80.1.27
-
Peduzzi P, Concato J, Kemper E, Holford TR, Feinstein AR. A simulation study of the number of events per variable in logistic regression analysis. J Clin Epidemiol. 1996;49(12):1373-9. https://doi.org/10.1016/S0895-4356(96)00236-3 PMID: 8970487
-
Altarawneh HN, Chemaitelly H, Ayoub HH, Tang P, Hasan MR, Yassine HM, et al. Effects of previous infection and vaccination on symptomatic Omicron infections. N Engl J Med. 2022;387(1):21-34. https://doi.org/10.1056/NEJMoa2203965 PMID: 35704396
-
Tartof SY, Xie F, Yadav R, Wernli KJ, Martin ET, Belongia EA, et al. Prior SARS-CoV-2 infection and COVID-19 vaccine effectiveness against outpatient illness during widespread circulation of SARS-CoV-2 Omicron variant, US Flu VE Network. Epidemiology. 2023.
-
Andrews N, Stowe J, Kirsebom F, Toffa S, Rickeard T, Gallagher E, et al. Covid-19 vaccine effectiveness against the omicron (b.1.1.529) variant. N Engl J Med. 2022;386(16):1532-46. https://doi.org/10.1056/NEJMoa2119451 PMID: 35249272
-
Tseng HF, Ackerson BK, Luo Y, Sy LS, Talarico CA, Tian Y, et al. Effectiveness of mRNA-1273 against SARS-CoV-2 Omicron and Delta variants. Nat Med. 2022;28(5):1063-71. https://doi.org/10.1038/s41591-022-01753-y PMID: 35189624
-
Kim SS, Chung JR, Talbot HK, Grijalva CG, Wernli KJ, Kiniry E, et al. Effectiveness of two and three mRNA COVID-19 vaccine doses against Omicron- and Delta-related outpatient illness among adults, October 2021-February 2022. Influenza Other Respir Viruses. 2022;16(6):975-85. https://doi.org/10.1111/irv.13029 PMID: 36825251
-
Kahn R, Schrag SJ, Verani JR, Lipsitch M. Identifying and alleviating bias due to differential depletion of susceptible people in postmarketing evaluations of COVID-19 vaccines. Am J Epidemiol. 2022;191(5):800-11. https://doi.org/10.1093/aje/kwac015 PMID: 35081612
-
Wong KLM, Gimma A, Coletti P, CoMix Europe Working GroupFaes C, Beutels P, et al. Social contact patterns during the COVID-19 pandemic in 21 European countries - evidence from a two-year study. BMC Infect Dis. 2023;23(1):268. https://doi.org/10.1186/s12879-023-08214-y PMID: 37101123
-
Tsang NNY, So HC, Cowling BJ, Leung GM, Ip DKM. Effectiveness of BNT162b2 and CoronaVac COVID-19 vaccination against asymptomatic and symptomatic infection of SARS-CoV-2 omicron BA.2 in Hong Kong: a prospective cohort study. Lancet Infect Dis. 2023;23(4):421-34. PMID: 36521506
-
Castelli JM, Rearte A, Olszevicki S, Voto C, Del Valle Juarez M, Pesce M, et al. Effectiveness of mRNA-1273, BNT162b2, and BBIBP-CorV vaccines against infection and mortality in children in Argentina, during predominance of delta and omicron covid-19 variants: test negative, case-control study. BMJ. 2022;379:e073070. https://doi.org/10.1136/bmj-2022-073070 PMID: 36450402
Data & Media loading...
Supplementary data
-
-
Supplement
-